Neural mechanisms of foraging

Abstract

Behavioral economic studies involving limited numbers of choices have provided key insights into neural decision-making mechanisms. By contrast, animals' foraging choices arise in the context of sequences of encounters with prey or food. On each encounter, the animal chooses whether to engage or, if the environment is sufficiently rich, to search elsewhere. The cost of foraging is also critical. We demonstrate that humans can alternate between two modes of choice, comparative decision-making and foraging, depending on distinct neural mechanisms in ventromedial prefrontal cortex (vmPFC) and anterior cingulate cortex (ACC) using distinct reference frames; in ACC, choice variables are represented in invariant reference to foraging or searching for alternatives. Whereas vmPFC encodes values of specific well-defined options, ACC encodes the average value of the foraging environment and cost of foraging.

Fig.1

A) Trials started with two central stimuli (encounter value), six alternative stimuli (search value) in a box at the top (drawn from a set of 12 learned in a previous session) while box color indicated current potential search cost. The horizontal bar indicated previously collected points. The first choice was a forage – to engage with the encounter value or search for an alternative. Searching led back to the initial screen with a new encounter value drawn from the previous set of alternatives. Engaging led to the second type of choice – the decision – between the two component stimuli that constituted the encounter value. The pseudo-randomly determined reward probabilities were now revealed. After the decision feedback indicated reward delivery. Factors (β-weights from logistic regressions) influencing likelihoods of search during forages (B) and picking the right stimulus during decisions (C).

Fig.2

ACC activity was higher in forages than decisions (A), better related to the inverse value difference (VD) during decisions than foraging(B), reflected the main effect of search value during foraging (C), and better related to search VD than decision VD (D). ACC time courses during engage (E) and search (F). (G) Individual peak ACC BOLD β-weights 5-10 s post-forage stimulus onset correlated with behavioral effects of the search value on search behavior (bottom) while ACC β-weights of best search value component predicted repeated searching (top). VmPFC exhibited no such correlations. (H) Time course for engage forages and the subsequent decision phase: The search value (red) signal continued into the decision phase. Reward magnitudes associated with chosen (green) and unchosen (orange) components of encounter value (left) were represented from their onset in the forage phase and into the decision phase. The reward probabilities of the chosen and unchosen options were only revealed after engaging and their BOLD effects therefore appear later (right).

Fig.3

(A) VmPFC time courses during forages (conventions as Fig.2e). (B) Activity better related to decision VD than to forage VD. (C) VmPFC time course for engage forages and the subsequent decision phase (conventions as Fig.2h). D) Individual peak vmPFC BOLD β-weights 5-10 s post-decision onset correlated with estimates of decision accuracy (softmax temperature).

Fig.4

Ventral striatal time courses after feedback following search forages (A). Effect of search costs when search is chosen (B). Individual peak BOLD β-weights for new encounter value (Ci) and peak BOLD β-weights for new search costs on searching (Cii) 5-10 s post-event onset both correlated with the proportion of forages on which participants searched. Increased coupling with left ventral striatum as a function of search cost during searches (D) and individual differences in foraging readiness (E) both revealed an ACC region anterior to, but overlapping with, that in Fig.2d.